Crossmodal links in endogenous and exogenous spatial attention: evidence from event-related brain potential studies

The adaptive control of behaviour in response to relevant external objects and events often requires the selection of information delivered by different sensory systems, but from the same region in external space. This can be facilitated by crossmodal links in the attentional processing of information across sensory modalities. Results from recent event-related potential (ERP) studies are reviewed that investigated mechanisms underlying such crossmodal links in spatial attention between vision, audition and touch. Crossmodal attention effects were observed for early modality-specific visual, auditory, and somatosensory ERP components, indicating that crossmodal links in spatial attention affect sensory-perceptual processes within modality-specific cortical regions. ERP modulations prior to target events but sensitive to the direction of an attentional shift were remarkably similar during anticipatory covert shifts of visual, auditory, or tactile attention. These results suggest that such attentional shifts are mediated by supramodal frontoparietal control mechanisms. Finally, ERP evidence is reviewed suggesting that effects of crossmodal links in endogenous (voluntary) as well as exogenous (involuntary) spatial attention are mediated by a representations of external space which are updated across postural changes.     

Spatio-temporal dynamics of top-down control: directing attention to location and/or color as revealed by ERPs and source modeling

This study investigated the nature and dynamics of the top-down control mechanisms that afford attentional selection using event-related potentials (ERPs) and dipole-source modeling. Subjects performed a task in which they were cued to direct attention to color, location, a conjunction of color and location or no specific feature on a trial-by-trial basis. Overall, similar ERP patterns were observed for directing attention to color and location, suggesting that spatial and non-spatial attention rely to a great extent on similar control mechanisms. The earliest attention-directing effect, at 340 ms, was localized to ventral posterior cortex and may reflect processes by which the cue is linked to its associated feature. Only late in the cue-target interval, differences in ERP were observed between directing attention to color and location. These originated from anterior and ventral posterior areas and may represent differences in, respectively, maintenance and perceptual biasing processes. The ventral posterior sources estimated for these late effects of directing attention to location and color were located posterior to those estimated for the modulatory effects of, respectively, spatial and non-spatial attention. This suggests that the precise neural populations involved in perceptual biasing and attentional modulation may differ. Conjunction cues initially elicited less posterior positivity than color and location cues, but evoked greater central positivity from 540 ms on. This central effect may reflect feature integration or ongoing processes related to cue-symbol translation. These results extend our understanding of the spatio-temporal dynamics of top-down attentional control.     

The processing of emotional facial expression is gated by spatial attention: evidence from event-related brain potentials

To investigate whether the processing of faces and emotional facial expression can be modulated by spatial attention, ERPs were recorded in response to stimulus arrays containing two faces and two non-face stimuli (houses). In separate trials, attention was focused on the face pair or on the house pair, and facial expression was either fearful or neutral. When faces were attended, a greater frontal positivity in response to arrays containing fearful faces was obtained, starting about 100 ms after stimulus onset. In contrast, with faces located outside the attentional focus, this emotional expression effect was completely eliminated. This differential result demonstrates for the first time a strong attentional gating of brain processes involved in the analysis of emotional facial expression. It is argued that while an initial detection of emotionally relevant events mediated by the amygdala may occur pre-attentively, subsequent stages of emotional processing require focal spatial attention. The face-sensitive N170 component was unaffected by emotional facial expression, but N170 amplitudes were enhanced when faces were attended, suggesting that spatial attention can modulate the structural encoding of faces.     

Feature-specific attention allocation overrules the orienting response to emotional stimuli

Emotional stimuli are generally thought to be processed in an unconditional fashion. Recent behavioral studies suggest, however, that emotional stimulus processing is critically dependent on attention toward emotional stimulus features. We set out to test this hypothesis using EEG measurements and a modified oddball paradigm. Unexpected emotional stimuli evoked amplitude variations of the P3a (an ERP marker of attention orienting) when attention was directed to emotional stimulus properties but not when non-emotional stimulus properties were attended to. We conclude that emotional stimulus processing is not unconditional, but dependent on top-down attentional control.     

Spatial attention: normal processes and their breakdown

Although "attention" is a general term in everyday folk and psychologic use, using research from cognitive psychology allows a focus on the processes associated with attention. A process-oriented definition of attention [2] makes "attention" a concept that can be studied rigorously. Attention is necessary for eliminating unwanted sensory inputs or irrelevant behavioral tasks and is useful when some cognitive system or process receives too many inputs. Attention acts to restrict the number of inputs and allow processing to continue in an effective manner. Although there are many forms of attentional selection, spatial attention is the most studied and perhaps the best understood form of selection. Spatial attention is the variety of attention most widely studied in neuropsychologic populations. As was evident from the authors' review, different neuropsychologic syndromes can be characterized as involving different difficulties with the component processes of spatial attention. Different neural structures work in concert to produce normal spatial selection, and damage to any of these neural structures, including the parietal and frontal lobes, pulvinar, and superior colliculus, produce an attentional impairment. Attentional impairments often have been studied in cases of focal brain damage resulting from stroke, traumatic brain injury, tumor, and surgical resection. Focal or multifocal lesions caused by neurodegenerative impairments, such as PSP and AD, however, also have marked effects on neural processes of attention. Patients with AD exhibit a range of impairments in spatial attention, and these impairments have been studied relatively little. Despite the understanding of attention provided by various patient populations, gaps remain in knowledge of the mechanisms involved in attending to space. For example, most studies of neurologic patients have used a simple spatial cuing paradigm with highly predictive cues. Although this task yields robust results and can be adapted for use with many different patient groups, the spatial cuing effects produced by such tasks have multiple interpretations (e.g., allocation of resources versus reduction of decision noise). This review highlights the general point that different neural sites seem to be responsible for different forms of attentional control, such as object-based attention, attentional task switching, and the executive control of attention [8.33]. Understanding the integration of these neural sites and their relationship to cognitive processes and, ultimately, behavior, will increase understanding of normal and disordered attentional selection.     

Selective attention to spatial frequency: an ERP and source localization analysis.

OBJECTIVES: Physiological correlates of visual selective attention have been observed by recording ERPs to attended versus ignored target stimuli. Over many such studies, spatial attention has been observed to modulate early sensory components beginning 70 ms after stimulus onset, while effects of selection based on other stimulus features such as color and spatial frequency occur at longer latencies. Together, these findings argue for a primacy of location in early attentional selection. However, there have been some reports suggesting attention effects on short latency sensory-evoked potentials during selection of spatial frequency. The prime objective of the present study was to assess whether or not spatial frequency-dependent potentials are modulated by attention at a latency as early as 70-100 ms. METHODS: Checkerboard patterns were flashed to the subject, one being the target requiring a response. We investigated attentional effects using high-density scalp mapping and inverse dipole modeling. RESULTS: The earliest robust signs of selective attention to spatial frequencies consisted of an occipital selection negativity (OSN) and a frontal selection positivity (FSP). The OSN started at a latency of 140 ms, the FSP somewhat earlier at 120 ms. These attention effects were readily modeled by sources in cortical areas ventrally and laterally to the more primary areas generating the shorter-latency sensory components. CONCLUSIONS: This pattern of results has been found for non-spatial stimulus features in several studies, and is clearly different from the ERP correlates of spatial selection.     

Attending to multiple visual streams: interactions between location-based and category-based attentional selection

Behavioral studies indicate that subjects are able to divide attention between multiple streams of information at different locations. However, it is still unclear to what extent the observed costs reflect processes specifically associated with spatial attention, versus more general interference due the concurrent monitoring of multiple streams of stimuli. Here we used a factorial design to disentangle the correlates of location- versus category-based selection processes during fMRI. In all conditions, participants were presented with two overlapping visual stimuli (red shapes and green shapes) in each hemifield. In different blocks, subjects either: (1) attended to one single stimulus category, red shapes or green shapes, in one hemifield; (2) attended to both stimulus categories in the same hemifield; (3) attended to one single stimulus category, but monitoring both hemifields at the same time; or (4) attended to one stimulus category in one hemifield, and the other category in the opposite hemifield. The behavioral data showed the expected costs of dividing spatial attention across the two hemifields, and the cost of monitoring two stimulus categories versus one category. The imaging data revealed activation of a dorsal fronto-parietal network, both for dividing spatial attention and for monitoring multiple stimulus categories. However, unlike behavioral data, the imaging results also showed a significant interaction between location- and category-based attention within the same network. This demonstrates that the fronto-parietal cortex engages in both of these selective attention functions, and that a mere increase in task difficulty cannot explain colocalization of these processes. We conclude that, under conditions of multiple streams monitoring, fronto-parietal regions control location- and category-based attentional selection.     

Emotional processing and its impact on unilateral neglect and extinction

Unilateral spatial neglect is a neurological disorder characterized by impaired orienting of attention to stimuli located in the contralesional space, typically following right-hemisphere damage. Neuropsychological investigations in the past two decades have demonstrated that neglect is caused by deficits affecting a widespread cortico-subcortical fronto-parietal network controlling spatial attention, but usually sparing early sensory pathways. As a consequence, certain residual abilities in sensory processing remain intact and still take place for stimuli in the neglected space, such as the extraction and organization of coherent or meaningful object features. Moreover, these residual abilities can alleviate inattention symptoms when contralesional stimuli are perceptually or biologically salient. Here we review recent studies suggesting that the emotional content of stimuli may also be processed despite impaired attention towards contralesional space, and that such processing may act to enhance attention and partly reduce neglect for these stimuli, relative to similar but emotionally neutral stimuli. For example, faces with emotional expressions, voices with emotional prosody, as well as pictures of scenes or even spiders have been found to be less severely extinguished from awareness in conditions of bilateral stimulations, and/or lead to fewer omissions in search tasks with multiple distracters. Gaze cues and reward learning might also produce similar effects. Altogether, these findings suggest that emotionally significant information is not only extracted from stimuli at neglected locations through spared pathways, but can also induce emotional biases in attention that partly counteract the abnormal spatial biases caused by fronto-parietal damage. We discuss results from neuropsychology and neuroimaging research suggesting that specific mechanisms for emotional attention might exist, centered on the amygdala and other limbic regions, and that these mechanisms can operate partly independent from other circuits controlling spatial and object-based attention. Although we are only beginning to understand these interactive effects of emotion and attention and to identify their neuroanatomical substrates, we believe that a deeper knowledge of such mechanisms and their conditions of optimal operation will help develop or improve therapeutic strategies in neglect patients.     

Objections against the view of visual extinction as an attentional disengagement deficit: the interaction between spatial position and temporal modulation

Visual extinction is a common consequence of brain injury where individuals fail to detect a contralesional target when it is presented with a competing ipsilesional target. This disorder is often seen as either a consequence of biased competitive interactions or as a consequence of an attentional disengagement deficit. A study of neurological patients by Rorden et al. (2008) found that extinction is maximal at stimulus simultaneity when the target stimuli straddle the central gaze fixation location, while it is maximal when the ipsilesional stimulus has a temporal lead on the contralesional stimulus when both target stimuli are presented in the ipsilesional visual field. The authors argued that these results are most parsimoniously explained as a consequence of low-level biased competitive interactions due to cortical magnification, but acknowledged that an attentional disengagement deficit could also accommodate the results. The present study set out to adjudicate between these models by examining the performance of neurologically healthy subjects who exhibit normal cortical magnification but do not have pathological attentional biases. We presented (a)synchronous double stimulation trials where both targets to be identified could straddle the central gaze fixation location or be presented in either the left or the right visual field. We found that in both the left and the right visual field target performance accuracy was poorest when the more peripheral stimulus led. This suggests that the findings from Rorden et al. can indeed be explained by a low-level physiological bias due to cortical magnification and argues against the notion that neurological extinction represents an attentional disengagement deficit.     

Testing cognitive models of visual attention with fMRI and MEG

Neuroimaging techniques can be used not only to identify the neural substrates of attention, but also to test cognitive theories of attention. Here we consider four classic questions in the psychology of visual attention: (i) Are some 'special' classes of stimuli (e.g. faces) immune to attentional modulation?; (ii) What are the information units on which attention operates?; (iii) How early in stimulus processing are attentional effects observed?; and (iv) Are common mechanisms involved in different modes of attentional selection (e.g. spatial and non-spatial selection)? We describe studies from our laboratory that illustrate the ways in which fMRI and MEG can provide key evidence in answering these questions. A central methodological theme in many of our fMRI studies is the use of analyses in which the activity in certain functionally-defined regions of interest (ROIs) is used to test specific cognitive hypotheses. An analogous sensor-of-interest (SOI) approach is applied to MEG. Our results include: evidence for the modulation of face representations by attention; confirmation of the independent contributions of object-based and location-based selection; evidence for modulation of face representations by non-spatial selection within the first 170 ms of processing; and implication of the intraparietal sulcus in functions general to spatial and non-spatial visual selection.     

ERP correlates of shared control mechanisms involved in saccade preparation and in covert attention

We investigated whether attention shifts and eye movement preparation are mediated by shared control mechanisms, as claimed by the premotor theory of attention. ERPs were recorded in three tasks where directional cues presented at the beginning of each trial instructed participants to direct their attention to the cued side without eye movements (Covert task), to prepare an eye movement in the cued direction without attention shifts (Saccade task) or both (Combined task). A peripheral visual Go/Nogo stimulus that was presented 800 ms after cue onset signalled whether responses had to be executed or withheld. Lateralised ERP components triggered during the cue-target interval, which are assumed to reflect preparatory control mechanisms that mediate attentional orienting, were very similar across tasks. They were also present in the Saccade task, which was designed to discourage any concomitant covert attention shifts. These results support the hypothesis that saccade preparation and attentional orienting are implemented by common control structures. There were however systematic differences in the impact of eye movement programming and covert attention on ERPs triggered in response to visual stimuli at cued versus uncued locations. It is concluded that, although the preparatory processes underlying saccade programming and covert attentional orienting may be based on common mechanisms, they nevertheless differ in their spatially specific effects on visual information processing.     

Orienting of attention in left unilateral neglect

After right posterior brain damage, patients may ignore events occurring on their left, a condition known as unilateral neglect. Although deficits at different levels of impairment may be at work in different patients, the frequency and severity of attentional problems in neglect patients have been repeatedly underlined. Recent advances in the knowledge of the mechanisms of spatial attention in normals may help characterizing these deficits. The present review focuses on studies exploring several aspect of attentional processing in unilateral neglect, with particular reference to the dichotomy between 'exogenous', or stimulus-related, and 'endogenous', or strategy-driven, orienting of attention. A large amount of neuropsychological evidence suggests that a basic mechanism leading to left neglect behavior is an impaired exogenous orienting toward left-sided targets. In contrast, endogenous processes seem to be relatively preserved, if slowed, in left unilateral neglect. Other component deficits, such as a general slowing of the operations of spatial attention, might contribute to neglect behavior. These results are presented and discussed, and their implications for hemispheric specialization in attentional orienting and for the mechanisms of visual consciousness are explored.     

Effects of attentional load on early visual processing depend on stimulus timing

A growing number of studies suggest that early visual processing is not only affected by low-level perceptual attributes but also by higher order cognitive factors such as attention or emotion. Using high-density electroencephalography, we recently demonstrated that attentional load of a task at fixation reduces the response of primary visual cortex to irrelevant peripheral stimuli, as indexed by the C1 component. In the latter study, peripheral stimuli were always presented during intervals without task-relevant stimuli. Here, we use a similar paradigm but present central task stimuli and irrelevant peripheral stimuli simultaneously while keeping all other stimulus characteristics constant. Results show that rather than to suppress responses to peripheral stimulation, high attentional load elicits higher C1 amplitudes under these conditions. These findings suggest that stimulus timing can profoundly alter the effects of attentional load on the earliest stages of processing in human visual cortex.     

Tracking the location of visuospatial attention in a contingent capture paradigm

Currently, there is considerable controversy regarding the degree to which top-down control can affect attentional capture by salient events. According to the contingent capture hypothesis, attentional capture by a salient stimulus is contingent on a match between the properties of the stimulus and top-down attentional control settings. In contrast, bottom-up saliency accounts argue that the initial capture of attention is determined solely by the relative salience of the stimulus, and the effect of top-down attentional control is limited to effects on the duration of attentional engagement on the capturing stimulus. In the present study, we tested these competing accounts by utilizing the N2pc event-related potential component to track the locus of attention during an attentional capture task. The results were completely consistent with the contingent capture hypothesis: An N2pc wave was elicited only by distractors that possessed the target-defining attribute. In a second experiment, we expanded upon this finding by exploring the effect of target-distractor similarity on the duration that attention dwells at the distractor location. In this experiment, only distractors possessing the target-defining attribute (color) captured visuospatial attention to their location and the N2pc increased in duration and in magnitude when the capture distractor also shared a second target attribute (category membership). Finally, in three additional control experiments, we replicated the finding of an N2pc generated by distractors, only if they shared the target-defining attribute. Thus, our results demonstrate that attentional control settings influence both which stimuli attract attention and to what extent they are processed.     

Explicit semantic stimulus categorization interferes with implicit emotion processing

Previous functional magnetic resonance imaging and event-related brain potential studies revealed that performing a cognitive task may suppress the preferential processing of emotional stimuli. However, these studies utilized simple and artificial tasks (i.e. letter, shape or orientation discrimination tasks), unfamiliar to the participants. The present event-related potential study examined the emotion–attention interaction in the context of a comparably more natural scene categorization task. Deciding whether a natural scene contains an animal or not is a familiar and meaningful task to the participants and presumed to require little attentional resources. The task images were presented centrally and were overlaid upon emotional or neutral background pictures. Thus, implicit emotion and explicit semantic categorization may compete for processing resources in neural regions implicated in object recognition. Additionally, participants passively viewed the same stimulus materials without the demand to categorize task images. Significant interactions between task condition and emotional picture valence were observed for the occipital negativity and late positive potential. In the passive viewing condition, emotional background images elicited an increased occipital negativity followed by an increased late positive potential. In contrast, during the animal-/non-animal-categorization task, emotional modulation effects were replaced by strong target categorization effects. These results suggest that explicit semantic categorization interferes with implicit emotion processing when both processes compete for shared resources.     

Dissociation between top-down attentional control and the time course of visual attention as measured by attentional dwell time in patients with mild cognitive impairment

Studies of the time course of visual attention have identified a temporary functional blindness to the second of sequentially presented stimuli in that the attentional cost of attending to one visual stimulus may lead to impairments in identifying a second stimulus presented within 500 ms of the first. This phenomenon is known as the attentional blink or attentional dwell time. The neural correlates of the attentional blink and its relationship to mechanisms that control attention are unknown. To examine this relationship we tested healthy controls and subjects in the preclinical stage of Alzheimer's disease, known as mild cognitive impairment (MCI), on a paradigm which affords quantification of both the attentional blink and the top-down control of attention. When subjects were asked to identify both a number and a letter that were rapidly and sequentially presented on a visual display, the detrimental effect that identifying the first stimulus had on the ability to identify the second served as a measure of the attentional blink. When asked to identify only one of the two stimuli, the ability to ignore the first stimulus was a function of their top-down attentional control. The MCI subjects demonstrated a normal attentional dwell time but in contrast they showed impaired top-down attentional control within the same paradigm. This dissociation suggests that these two aspects of visual attention are subserved by different neural systems. The possible neural correlates of these two attentional functions are discussed.     

The Microgenesis of Global Perception in Autism

Several studies have reported that individuals with autism and Asperger’s syndrome show a local processing bias on tasks involving features and configurations. This study assessed whether this bias results from differences in the perception of features or a cognitive bias to attend to features in autism as a consequence of a deficit in attending to configurations. Children with autism and typically developing children performed a task assessing the initial perceptual representation of features and configurations following a 50 ms stimulus display and the development of the perceptual representation by grouping processes following an 800 ms stimulus display. No differences were observed between the two groups, suggesting that the perceptual and attentional mechanisms marshalled by this task operate typically in children with autism.     

Does attention affect the motor programs of pharmacologically induced eye movements?

Attention plays an important role in oculomotor function. We studied the effect of attentional stimuli on eye movements induced by ketamine. The experiments were carried out on three monkeys. Ketamine injected intramuscularly induced nystagmus. When we switched on a new stimulus these eye movements stopped and the animal made a saccade toward it. This may be due to a new motor program, triggered by a visual stimulus, that among its characteristics is able to engage the animal's attention. The program of evoked saccade is overwritten on induced oculomotor activity. Our results suggest that attentional processes modify the dynamic characteristics and induce in particular behavioral condition a new motor program.     

Hemispheric modulations of alpha-band power reflect the rightward shift in attention induced by enhanced attentional load

Rightward shifts in attention are a common consequence of brain injury. A growing body of evidence appears to suggest that increases in attentional load, and decreases in alertness can lead to rightward shifts in attention in healthy and patient populations. It is unclear however whether these factors affect spatial biases in attention at the level of preparatory control processes or at the level of stimulus driven expression mechanisms. Whilst such effects cannot easily be dissociated behaviourally, the robust association between changes in α-band activity and shifts in visual attention provides a neural marker by which the temporal dynamics of effects of attentional load on spatial processing might be examined. Here we use electroencephalography to examine the relationship between modulations in α-band activity and behavioural outcome on a dual task paradigm comprising a detection task (t1), closely followed by a temporal order judgment task (t2). We examine the effects of high (respond to t1 and t2) and low (t2 only) attentional load conditions on spatial bias and changes in lateralization of α-band activity over the course of the trial. As anticipated a rightward bias in detecting target onsets was observed in the temporal order judgment task (t2) under conditions of high attentional load. This rightward shift in attention was associated with changes in the lateralization of α-band activity that occurred only after the presentation of t2, suggesting that attentional load may primarily influence expression mechanisms.     

Voluntary and involuntary spatial attentions interact differently with awareness

Although the nature of the relationship between attention and awareness is actively debated, the possibility that different forms of attention might interact differently with awareness has never been directly tested. We examine here whether voluntary and involuntary spatial attentions, two forms of attention that were distinguished by manipulating the predictability of central arrow cues, interact in the same way with visual awareness. Conscious perception was enhanced by both voluntary and involuntary attentions, and to a similar extent, suggesting volition may not be an essential feature for awareness. However, the influence of attention was dependent on the awareness of the target stimulus: Voluntary attention shortened reaction times and improved discrimination accuracy of cued relative to uncued stimuli, but only when the stimuli were consciously perceived. Involuntary attention shortened reaction times for cued relative to uncued target stimuli, but only when the stimuli were not consciously perceived. Our results imply that the nature of the relationship between attention and awareness is not a simple one but depends on the type of attention involved. More specifically, our results suggest that the aware or unaware status of the stimulus could determine whether attentional facilitation is driven by voluntary or involuntary mechanisms, a proposal that goes in the opposite direction of the classical view that attention controls awareness. Because voluntary attentional benefits were observed in aware trials but involuntary attentional benefits were observed in unaware trials only, our results also argue against the idea that attentional effects on conscious and unconscious processing are fundamentally of the same nature.